Antimicrobial resistance pattern of bovine, poultry, and porcine MRSA isolates.
Abstract
Methicillin-resistant Staphylococcus aureus (MRSA) has become a growing concern in companion and food-producing animals. The presence of multidrug-resistance with a wide range of extracellular enterotoxin genes, virulence factors, and Panton-Valentine leukocidin (pvl) cytotoxin genes confer life-threatening traits on MRSA and makes them highly pathogenic and difficult to treat. Clonal complex 398 (CC398), a predominant clonal lineage of livestock-associated-MRSA in domestic animals and retail meat, is capable of infecting humans. In order to monitor and prevent MRSA contamination, it is critical to understand its source and transmission dynamics. In this review, we describe MRSA in food-producing animals (pig, cattle, chicken), horses, pet animals (dogs, cats), and food products (pork, beef, chicken, milk, and fish).
Keywords
- MRSA
- companion animals
- food-producing animals
- food products
- CC398
1. Introduction
LA-MRSA was first detected in milk with bovine mastitis from Belgium in 1972 [11–13]. Thereafter, MRSA reports in various food and companion animals, such as pigs, cattle, chickens, dogs, cats, and horses, have increased [11, 14]. A novel strain of MRSA belonging to multilocus sequencing type (MLST) 398 (ST398) and related strains collectively grouped into clonal complex 398 (CC 398) have been frequently found in pigs, chickens, veal calves, dairy cattle, horses, dogs, and milk in various countries [11]. Both methicillin-susceptible
LA-MRSA infections among livestock animals and associated farmers are of great concern as these sources could potentially serve as reservoirs for zoonotic infections [14]. Contamination of food with enterotoxin producing
2. MRSA in food-producing animals
2.1. Porcine MRSA
In 2005, pigs were reported as an animal reservoir of
Various farm types in the Netherlands were reported to have MRSA in 23–71% of their pigs, and it was especially high in farms with finishing pigs (pigs are almost ready to be sent to market) [49, 57, 64]. The presence of MRSA is dependent on pig production type and herd size and increases from 31 to 86% depending upon small-, medium-, and large-sized farms carrying <250, >500, and >1000 animals, respectively [45, 62, 64, 65]. MRSA prevalence also varied with farm type, e.g., fattening and closed (farrow-to-finish) farms exhibited 94 and 56% MRSA, respectively [66]. Transportation from farm to slaughterhouse [38, 67], lairage [38], national and international trade [57], and slaughter house employees all have been reported to enhance MRSA contamination and may play important roles in transmission of the bacteria [68]. It was proposed that MRSA contamination in piglets is dependent on the status of sows [69]. When a sow was colonized with MRSA, 100% piglets were MRSA-positive. However, 84% piglets were MRSA-positive when there was no MRSA contamination in a sow. Higher numbers of MRSA were isolated in suckling (52.9%) and weanling piglets (53.4%) than sows (38.3%) [64]. Prevalence of MRSA in pigs has been linked to their age but the data are not conclusive. MRSA were identified in 100% of 9–12-week-old pigs, whereas in adult animals it decreased to 36% [51]. On the other hand, Weese et al. [69] reported that MRSA was more prevalent in post-weaning (85%) than preweaning pigs (34.5%) in pig farms without antimicrobial treatment. Percent of MRSA colonization in Canadian piglets on days 1, 28, 56, and 70 were 1, 34, 50, and 42%, respectively [69]. Khanna et al. [60] reported no variation in MRSA prevalence based on age groups. MRSA does not seem to cause serious infection in pigs, but there have been a few reports of MRSA from exudative epidermitis lesions of piglets on a breeding farm [70] and in pigs suffering from infection of the urinary-genital tract, skin infection, and metritis-mastitis-agalactia syndrome [71]. While MRSA ST398 isolated from diseased pigs did not carry the major virulence genes, such as toxic shock syndrome toxin 1,
The epidemiology of livestock-associated
2.2. Bovine MRSA
The first report of MRSA in farm animals was published in the early 1970s, when the bacteria were isolated from the milk of dairy cows with mastitis in Belgium [86] and clustered in the CC398 group [87]. Devriese and Hommez [88] suspected that these samples were most likely contaminated by humans. In the past few years, MRSA has been isolated from cows or their milk in Korea [89–91], Hungary, Mexico, and the Netherlands [89, 92, 93]. There have also been numerous reports of MRSA from cows or their milk in Brazil, Italy, Pakistan, Nigeria, Turkey, and the USA [94–96]. Subsequently, several reports have described bovine udder infections caused by LA-MRSA CC398 [97]. In Dutch farms, MRSA was detected in 18–31% of veal calves [98]. In 2010, the European Union reported that 20% of veal calves in Germany carried MRSA [99]. A survey of 51 veal calf farms in the Netherlands indicated that an average of 38% of farmers and 16% of family members were colonized with LA-MRSA [19, 100]. Recently, another group of LA-MRSA strains (CC130, CC425, and CC1943) that were initially thought to be bovine-specific lineages emerged in humans [101]. A number of multidrug-resistant MRSA were isolated from bovine mastitis in Germany [97, 102], the majority of which were MRSA ST398 related to animal strains, but an isolate of the clonal complex group CC8 was identified as a human epidemic MRSA strain Irish-01 [103]. In 2010, Hata et al. first discovered MRSA in cow’s milk in Japan and the genotypes (ST5-SCC
While a majority of the MRSA collected from dairy cattle belonged to ST398 [89], other ST types, such as ST1-t286-SCC
2.3. Poultry MRSA
CC398 is not limited to large livestock animals alone; it has also been reported in poultry [18, 122], manure from chicken farms and soil fertilized with this manure [123]. However, the numbers of MRSA ST398-t011-SCC
2.4. Other meat products
2.5. Milk
In general, the occurrence of MRSA in bovine mastitis isolates is well studied and its prevalence seems to be very low [140]. Following the initial reports of isolation of MRSA from mastitic cows [86], sporadic cases of MRSA in dairy cattle were detected among
2.6. Fish
Fish is not a normal host for staphylococci and its presence on fish is either due to disease in the fish, contamination, or poor personnel hygiene. The first report of the isolation of MRSA from Tilapia was published in 2010, where 559
3. MRSA in food processing environment
After carcasses leave the slaughter-house chillers, residual MRSA on carcass surfaces can be transmitted during further processing through human hands, cutting tools, and any surfaces with direct meat contact. Manual handling during processing also can facilitate the entry of human MRSA strains into the production units. Recent surveillance data suggest that 22.5–64.8% of retail beef, pork, chicken, and turkey meats in five different geographical locations in the United States were contaminated with
To pin point the exact source of contamination, it is necessary that the process of slaughtering be analyzed critically. Slaughter and meat processing involve several steps, any of which could introduce contamination with MRSA. Scalding, the first step in the slaughter process, is carried out at 60–62°C for 6–8 min in scalding tanks with rotating bars or through long scalding tanks [153] to loosen the hair from the carcass. An analysis of the effect of scalding on the quantity of coagulase-positive
4. Molecular epidemiology of S. aureus CC398
The emergence of LA-MRSA strains in humans [16, 17, 25, 56] and the presence of an identical MRSA CC398 in pigs, farm workers, veterinarians who attended to the same pig farms and their nonexposed family members [47, 48] suggests animal-to-human or human-to-animal transmission. In an interesting report from the Netherlands, it was shown that farm visitors were positive for CC398 MRSA directly after a farm visit but tested MRSA negative after 24 h [19, 41]. These and other studies indicate that CC398 appears to be frequently shared between animals and humans and is capable of causing infections in both species [25, 70, 164]. Transmission of MRSA between animals and humans is not new, but the MRSA isolates, in most cases, represent an initial human-to-animal transmission [24, 49, 165, 166].
Analysis of MRSA and MSSA from animals and humans spanning 19 countries and four continents indicated that the CC398 lineage originated in humans as an MSSA [167]. The whole-genome sequencing analysis by Price et al. [167] demonstrated that livestock-associated MRSA CC398 lost an immune-evasion cluster (IEC) as it evolved from its human-adapted MSSA. All of the HA-MSSA strains carry ØSa3 prophage in association with human innate immunomodulatory genes that play crucial roles in human niche adaptation (Figure 2) [167]. The prophage-associated virulence and adaptation genes are not necessary for nonhuman hosts, therefore, ØSa3 is mostly absent in livestock strains. After their introduction to livestock, MSSA CC398 acquired resistance to methicillin and tetracycline. Since tetracycline is heavily used in animal farming, the tetracycline resistance gene
It is quite possible that LA-MRSA CC398 strains would eventually acquire certain genetic traits (additional antibiotic resistance and virulence factors) that would allow
Bayesian phylogenetic analysis of the poultry isolates with the CC5 clade indicated that it arose due to a single human-to-poultry host jump in or near Poland, where CC5 poultry strains acquired an MGE (mobile genetic element), presumably from other resident staphylococcal strains [36]. In addition to gene acquisition, loss of staphylococcal protein A (SpA) has occurred in avian isolates; it encodes virulence factors involved in human disease pathogenesis but is not needed for avian pathogenesis. The lack of protein A expression is a characteristic of the poultry biotype as defined by Devriese et al. [148]. In addition to the CC5 poultry clade, several other poultry isolates had identical or closely related STs to strains commonly associated with humans but had acquired MGE unique to avian strains, indicating that human-to-poultry host switches may be happening relatively frequently. A recent study demonstrated frequent contamination of poultry meat products with
5. ST398 evolution and genetic diversity
In spite of similarities between LA- and HA-MRSA isolates, significant amounts of genetic diversity among
6. MRSA in companion animals
6.1. Canine and feline MRSA
The first MRSA from pet animals was isolated from dogs in Nigeria in 1972 [188].
MRSA isolates from Austria, Belgium, Germany, Ireland, and Portugal were resistant to ciprofloxacin and enrofloxacin, perhaps because of the fluoroquinolone approval for use in companion animals in Europe in the middle of 1990 (Table 2). MRSA ST398 that was identified in dogs and cats in France carried a chloramphenicol acetyltransferase gene,
Country | Animal | ST | AMP | CEF | CHL | CIP | CLI | ENR | ERY | FLO | FUS | GEN | KAN | LIN | LIZ | QD | SPE | STR | TET | TIA | TOB | TRI | SXT | Genotype | References |
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Belgium | B† | 398 | * | +** | + | + | + | + | + | + | + | + | [87] | ||||||||||||
Belgium | B | 398 | + | + | + | + | + | + | + | + | + | [133] | |||||||||||||
Belgium | C† | 239, 398 | + | + | + | + | + | + | + | + | + | + | + | + | [34] | ||||||||||
Belgium | C | 398 | + | + | + | + | + | [133] | |||||||||||||||||
Belgium | P† | ST9, 80, 239, 398 | + | + | + | + | + | + | + | + | + | + | + | + | + | + | [121] | ||||||||
Belgium | P | 398 | + | + | + | + | + | + | + | + | [256] | ||||||||||||||
Belgium | P | 398 | + | + | + | + | + | + | + | + | + | + | [66] | ||||||||||||
Belgium | P | 398 | + | + | + | + | + | + | + | + | + | + | [133] | ||||||||||||
Brazil | B | 398 | + | + | + | + | + | + | + | [257] | |||||||||||||||
Central Europe | P | 9 | + | + | + | + | + | [258] | |||||||||||||||||
China | P | 6, 9, 63, 627 | + | + | + | + | + | + | + | + | + | + | [259] | ||||||||||||
China | P | 5, 9 | + | + | + | + | + | + | + | [260] | |||||||||||||||
China | P | NA | + | + | + | + | + | + | + | + | [261] | ||||||||||||||
China | P | 398 | + | + | + | + | + | + | + | + | + | [262] | |||||||||||||
Finland | P | 1, 398 | + | + | + | + | + | [120] | |||||||||||||||||
Germany | B | 398 | + | + | + | + | + | + | + | + | + | + | + | + | [97] | ||||||||||
Germany | B | 398 | + | + | + | [102] | |||||||||||||||||||
Germany | P | 398 | + | + | + | + | + | + | + | + | + | + | + | + | + | [44] | |||||||||
Hong Kong | C | 9 | + | + | + | + | + | + | + | + | + | + | + | + | + | + | + | + | + | [134] | |||||
Hong Kong | P | 9 | + | + | + | + | + | + | [81] | ||||||||||||||||
Hong Kong | P | 9 | + | + | + | + | + | + | + | + | + | + | + | [134] | |||||||||||
Hong Kong | P | 9 | + | + | + | + | + | + | + | + | [263] | ||||||||||||||
Hungary | B | 1 | + | + | [92] | ||||||||||||||||||||
Ireland | P | CC398 | + | + | + | + | + | + | + | + | + | + | [264] | ||||||||||||
Italy | B | CC97 | + | + | + | + | + | + | + | + | + | + | + | [110] | |||||||||||
Italy | B | 1 | + | + | + | + | + | + | + | + | + | [119] | |||||||||||||
Italy | P | 1, 9, 97, 398, 1476 | + | + | + | + | + | + | + | + | + | [62] | |||||||||||||
Italy | P | CC97 | + | + | + | + | + | + | + | + | + | + | + | [110] | |||||||||||
Italy | P | 1 | + | + | + | + | + | + | + | + | + | + | [119] | ||||||||||||
Italy & Spain | P | 1 | + | + | + | + | + | + | + | + | + | [265] | |||||||||||||
Korea | B | NA | + | + | + | + | + | + | + | + | [89] | ||||||||||||||
Korea | B | 1, 72 | + | + | + | [108] | |||||||||||||||||||
Korea | B | NA | + | + | + | + | + | + | [90] | ||||||||||||||||
Korea | C | 692 | + | + | + | + | [91] | ||||||||||||||||||
Korea | C | NA | + | + | + | + | [89] | ||||||||||||||||||
Korea | P | 398 | + | + | + | + | [85] | ||||||||||||||||||
Korea | P | 5, 72, 398, 541 | + | + | + | + | + | + | + | + | + | + | + | [91] | |||||||||||
Netherland | B | 398 | + | + | + | + | + | [266] | |||||||||||||||||
Netherlands | P | 398 | + | + | + | + | + | + | [22] | ||||||||||||||||
Netherlands | P | 398 | + | + | + | + | + | [70] | |||||||||||||||||
Portugal | B | 398 | + | + | + | + | + | + | + | [206] | |||||||||||||||
Portugal | P | NA | + | + | + | + | + | + | + | + | + | [206] | |||||||||||||
Spain | P | 398, 1379 | + | + | + | + | + | + | + | + | [255] | ||||||||||||||
Spain | P | 398 | + | + | + | + | + | [234] | |||||||||||||||||
Spain | P | 1, 398, 1965, 1966, 1967, 1968, 1969 | + | + | + | + | + | + | + | + | + | + | + | [267] | |||||||||||
Switzerland | B | 1, 398 | + | + | + | + | + | [42] | |||||||||||||||||
Switzerland | P | 398 | + | + | + | + | + | + | + | [42] | |||||||||||||||
Switzerland | P | 398 | + | + | + | + | + | + | [63] | ||||||||||||||||
Taiwan | P | 9 | + | + | + | + | + | + | + | [268] | |||||||||||||||
Thailand | P | 9 | + | + | + | + | + | + | [31] | ||||||||||||||||
Thailand | P | 9, 2136 | + | + | + | + | + | + | + | + | [269] | ||||||||||||||
USA | P | 398 | + | + | + | + | [51] | ||||||||||||||||||
USA | P | 5, 72, 398, 1340 | + | + | + | + | + | + | + | [38] |
Country | Animal | ST | AMP | CEF | CHL | CIP | CLI | ENR | ERY | FLO | FUS | GEN | KAN | LIN | LIZ | QD | SPE | STR | TET | TIA | TOB | TRI | SXT | Genotype | References |
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Austria | D† | 22, 254, 398 | * | +** | + | + | + | + | [208] | ||||||||||||||||
Austria | C† | 1, 5, 398 | + | + | + | + | + | [208] | |||||||||||||||||
Austria | H† | 1, 254, 398 | + | + | + | + | + | + | [208] | ||||||||||||||||
Austria | H | 1, 254, 398 | + | + | + | + | [222] | ||||||||||||||||||
Belgium | D | 398 | + | + | + | + | + | + | + | + | + | [133] | |||||||||||||
Belgium | C | 398 | + | + | + | + | + | + | [133] | ||||||||||||||||
Belgium | H | 8, 398, 2197 | + | + | + | + | + | + | + | + | + | [270] | |||||||||||||
Belgium | H | 398 | + | + | + | + | + | + | [229] | ||||||||||||||||
Brazil | C | 30 | + | [204] | |||||||||||||||||||||
Brazil | C | NA | + | [193] | |||||||||||||||||||||
Canada | D | NA | + | + | + | + | + | + | + | + | + | [271] | |||||||||||||
Canada & USA | H | NA | + | + | + | + | + | + | [272] | ||||||||||||||||
China | C, D | 59, 398 | + | + | + | [273] | |||||||||||||||||||
France | C, D | CC398 | + | + | + | + | + | + | + | + | + | [117] | |||||||||||||
Germany | C, D, H | CC5, 8, 9, 22, 398, 599 | + | + | + | + | + | + | + | + | [274] | ||||||||||||||
Germany | C | 398 | + | + | + | + | + | + | + | + | + | + | [207] | ||||||||||||
Germany | C, D | 22 | + | + | + | + | [210] | ||||||||||||||||||
Germany | H | 8, 22, 254, 1117 | [183] | ||||||||||||||||||||||
Hong Kong | D | NA | + | + | + | + | + | + | + | + | [275] | ||||||||||||||
Ireland | D | NA | + | + | + | + | + | [276] | |||||||||||||||||
Ireland | D | NA | + | + | + | + | + | [226] | |||||||||||||||||
Ireland | H | NA | + | + | + | + | + | + | + | + | + | [226] | |||||||||||||
Israel | H | 5 | + | + | + | + | [277] | ||||||||||||||||||
Israel | H | 5 | + | + | + | + | [278] | ||||||||||||||||||
Japan | D | 5, 30 | + | + | + | + | + | + | [279] | ||||||||||||||||
Japan | D | NA | + | + | + | + | [280] | ||||||||||||||||||
Korea | D | 72 | + | [281] | |||||||||||||||||||||
Korea | D | NA | + | + | + | + | + | + | + | [282] | |||||||||||||||
Malaysia | D | 59 | + | + | + | + | [283] | ||||||||||||||||||
Malaysia | C | 55 | + | + | + | + | + | [283] | |||||||||||||||||
Netherlands | D | NA | + | + | + | + | + | [284] | |||||||||||||||||
Nigeria | D | NA | + | + | + | + | + | + | + | + | [285] | ||||||||||||||
Portugal | D | 22, 105, 398 | + | + | + | + | + | + | + | [206] | |||||||||||||||
Portugal | C | 5, 22 | + | + | + | + | [206] | ||||||||||||||||||
Portugal | D | 22 | + | + | + | + | + | + | + | + | + | [286] | |||||||||||||
Portugal | H | 5, 398 | + | + | + | + | + | + | + | [287] | |||||||||||||||
Portugal | H | 5 | + | + | + | + | + | + | + | + | [206] | ||||||||||||||
Switzerland | H | 8, 398 | + | + | + | + | + | + | + | + | [288] | ||||||||||||||
Thailand | D | 45 | + | + | + | + | + | + | + | + | + | + | [205] | ||||||||||||
USA | D | 5 | + | + | + | + | [289] | ||||||||||||||||||
USA | D | NA | + | + | + | + | + | + | + | + | [290] | ||||||||||||||
USA | D | 5, 8, 105, 986 | + | + | + | + | + | [118] | |||||||||||||||||
USA | C | 5, 8 | + | + | + | + | [118] | ||||||||||||||||||
USA | C | NA | + | + | + | + | + | + | [291] | ||||||||||||||||
USA | D | NA | + | [291] | |||||||||||||||||||||
USA | C, D | NA | + | + | + | + | + | + | + | [292] | |||||||||||||||
USA | D | NA | + | + | + | + | [293] | ||||||||||||||||||
USA | C | NA | + | + | + | + | [293] | ||||||||||||||||||
USA | C | NA | + | + | + | + | + | + | + | [216] | |||||||||||||||
USA & UK | D | NA | + | + | + | + | + | + | + | [294] | |||||||||||||||
USA | H | 8, 830 | + | + | + | + | + | [118] |
Country | Animals | Leukotoxins | Hemolysins | Enterotoxins | Immune-invasion factors | Protease | Superantigen-like proteins | Biofilm-associated | Capsule | Miscellaneous genes | References |
---|---|---|---|---|---|---|---|---|---|---|---|
Austria | Horses | [208] | |||||||||
Dogs | |||||||||||
Cats | |||||||||||
Belgium | Pigs | [121] | |||||||||
China | Pigs | [260] | |||||||||
Finland | Pigs | [120] | |||||||||
France | Cats and dogs | [117] | |||||||||
Germany | Pigs | [44] | |||||||||
Horses | [183] | ||||||||||
Italy | Cattle | [119] | |||||||||
Pigs | |||||||||||
Italy & Spain | Pigs | [265] | |||||||||
Korea | Pigs | [91] | |||||||||
Chicken | – | – | |||||||||
Cattle | |||||||||||
Portugal | Pigs | – | – | [206] | |||||||
Dog | |||||||||||
Horse | |||||||||||
Calf | – | – | |||||||||
Spain | Pigs | [255] | |||||||||
Switzerland | Pigs | [42] | |||||||||
Calf | |||||||||||
Cattle | |||||||||||
Thailand | Pigs | [269] | |||||||||
USA | Dogs | [118] | |||||||||
Cats | |||||||||||
Horses |
6.2. Equine MRSA
Since the first report of MRSA from mares with metritis in Japan [217], many isolates have been found in Europe, North America, and Asia (Table 2) [142–144, 218–220]). Haenni et al. [221] identified four
6.3. Antibiotic resistance and enterotoxin genes in LA-MRSA CC398
An analysis of MRSA and MSSA from animals and humans spanning 19 countries and four continents indicated that the CC398 lineage originated in humans as MSSA [167]. After its transmission to livestock, CC398 became resistant to tetracycline, probably because of the heavy tetracycline use in pig production [22]. However, many tetracycline-resistant MRSA strains are found in horses despite the fact that tetracycline is either not used much [229] or sparingly used [93, 229]. Among bovine MRSA isolates tested, most of them were resistant to β-lactam antibiotics [34] as well as tetracycline, erythromycin and gentamicin. CC398 has also been reported to be highly resistant to several other antibiotics, such as ciprofloxacin, tobramycin, clindamycin, and trimethoprim-sulfamethoxazole [234]. Antimicrobial resistance patterns of MRSA and MSSA isolates in Hong Kong were very similar [81]. The only MRSA CC398 isolate that has exhibited resistance against daptomycin and intermediate susceptibility to vancomycin has been described in a case-report from an Italian hospital [235]. Two other isolates, one from a ventilator-associated pneumonia of a farmer and one additional porcine isolate, were also described as resistant to linezolid and possessed the
About 50% of LA-MRSA CC398 isolates, besides being resistant to antimicrobial agents, also exhibit resistance to copper and zinc mediated by the
Most of the animal isolates are negative for the
7. Conclusions
MRSA contamination in food-producing and companion animals poses a serious threat to public health. Incidences of identical LA-MRSA strains in pig farms and persons in close contact with food producing and companion animals suggest a clear link for transmission of these strains between humans and animals. While MRSA isolates from companion and food-producing animals are known to infect humans, the reverse is also true. Studies reviewed in this report indicate an initial transfer of MSSA from humans to animals by deletion of immunomodulatory genes and prophage ØSa3, necessary for human infection but not required for infection in animals, and acquisition of tetracycline and methicillin resistance genes (Figure 2). The MRSA that evolved in animals started showing up in humans that were in close contact with them and exhibited traits specifically found in animal isolates, indicating a reverse transmission from animals to humans. Initial reports of MRSA in animals did not indicate the presence of host adaptation, enterotoxin, virulence, and antimicrobial resistance genes in them but they are becoming more prevalent and it is feared that these animals could serve as a reservoir for such strains and play an important role in zoonotic transfers.
Documentation of MRSA isolates (ST59-t437–V) from cattle containing the
A comprehensive study of the emergence, dissemination, prevention and control of MRSA colonization is required to mitigate the risks to both animal and human health. Rapid advancement of whole genome sequencing technology has the great power of discriminating closely associated MRSA isolates from different sources and could be used for source tracking and differentiating between animal and human origin isolates. In addition, it can be applied to monitor the emergence and dissemination of MRSA isolated from various environments and determine the characteristics of virulence factors and evolution of multi-antimicrobial resistance.
Disclaimer
The views expressed herein do not necessarily reflect those of the US Food and Drug Administration or the US Department of Health and Human Services.
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